Selection on gamete recognition proteins depends on sex, density, and genotype frequency.

Gamete recognition proteins can evolve at astonishing rates and lie at the heart of reproductive isolation and speciation in diverse taxa. However, the source of selection driving this evolution remains unknown. We report on how the sperm bindin genotype influences reproductive success under natural conditions. An interaction between genotype frequency and spawning density determines how sperm bindin genotype influences reproductive success. Common genotypes are selected under sperm-limited conditions, whereas rare genotypes are selected under conditions of intense sperm competition and sexual conflict. Variation in the evolutionary rates of bindin may reflect historic differences in sperm availability.